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Countershading in Zebrafish Results from an Asip1 Controlled

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Countershading in Zebrafish Results from an Asip1 Controlled www.nature.com/scientificreports OPEN Countershading in zebrafsh results from an Asip1 controlled dorsoventral gradient of pigment Received: 1 October 2018 Accepted: 12 February 2019 cell diferentiation Published: xx xx xxxx Laura Cal1, Paula Suarez-Bregua1, Pilar Comesaña1, Jennifer Owen2, Ingo Braasch3, Robert Kelsh 2, José Miguel Cerdá-Reverter4 & Josep Rotllant1 Dorso-ventral (DV) countershading is a highly-conserved pigmentary adaptation in vertebrates. In mammals, spatially regulated expression of agouti-signaling protein (ASIP) generates the diference in shading by driving a switch between the production of chemically-distinct melanins in melanocytes in dorsal and ventral regions. In contrast, fsh countershading seemed to result from a patterned DV distribution of diferently-coloured cell-types (chromatophores). Despite the cellular diferences in the basis for counter-shading, previous observations suggested that Agouti signaling likely played a role in this patterning process in fsh. To test the hypotheses that Agouti regulated counter-shading in fsh, and that this depended upon spatial regulation of the numbers of each chromatophore type, we engineered asip1 homozygous knockout mutant zebrafsh. We show that loss-of-function asip1 mutants lose DV countershading, and that this results from changed numbers of multiple pigment cell-types in the skin and on scales. Our fndings identify asip1 as key in the establishment of DV countershading in fsh, but show that the cellular mechanism for translating a conserved signaling gradient into a conserved pigmentary phenotype has been radically altered in the course of evolution. Most vertebrates exhibit a dorso-ventral pigment pattern characterized by a light ventrum and darkly colored dorsal regions. Tis countershading confers UV protection against solar radiation, but also is proposed to pro- vide anti-predator cryptic pigmentation. In mammals, hair color results from biochemical diferences in the melanin produced by melanocytes, the only neural-crest derived pigment cell-type in this taxon. Best studied in mice, the local expression of agouti-signaling protein (ASIP) in the ventral skin drives the dorso-ventral pig- ment polarization1,2. ASIP is mainly produced by dermal papillae cells where it controls the switch between production of eumelanin (black/brown pigment) to pheomelanin (yellow/red pigment) by antagonizing α-melanocyte-stimulating hormone (α-MSH) stimulation of the melanocortin 1 receptor (MC1R)1. Temporal control of Asip expression as a pulse midway during the hair growth cycle generates a pale band of pheomelanin in an otherwise dark (eumelanin) hair (‘agouti’ pattern). In contrast, in the ventral region, constitutive expression of Asip at high levels represses eumelanin production, resulting in pale hair colour. Most other groups of vertebrates share the dorso-ventral countershading pattern, but in ray-fnned fshes it results from a patterned distribution of light-refecting (iridophores and leucophores) and light-absorbing (mel- anophores, xanthophores, erythrophores, and cyanophores) chromatophores3,4. Zebrafsh, a teleost fsh model for pigment studies, obtains its striped pigmentation by the patterned distribution of three types of chromatophores: melanophores, iridophores and xanthophores5,6. Furthermore, it is widely accepted that fsh melanophores only produce dark eumelanin, but not pheomelanin7. Our recent experiments using overexpression systems have demonstrated that zebrafsh utilizes two distinct adult pigment-patterning mechanisms, the striped pattern- ing mechanism and the dorso-ventral patterning mechanism8. Both patterning mechanisms function largely 1Deparment of Biotechnology and Aquaculture. Instituto de Investigaciones Marinas, IIM-CSIC, Vigo, 36208, Spain. 2Department of Biology and Biochemistry and Centre for Regenerative Medicine, University of Bath, Claverton Down, Bath, BA2 7AY, United Kingdom. 3Department of Integrative Biology and Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI, 48824, USA. 4Instituto de Acuicultura de Torre de la Sal, IATS-CSIC, Castellón, 12595, Spain. Correspondence and requests for materials should be addressed to J.R. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:3449 | https://doi.org/10.1038/s41598-019-40251-z 1 www.nature.com/scientificreports/ www.nature.com/scientificreports independently, with the resultant patterns superimposed to give the full pattern8. Te zebrafsh striping mecha- nism has received much attention and is based on a cell-cell interaction mechanism9,10. In contrast, dorso-ventral patterning has been largely neglected, but we have recently provided evidence that it depends on asip1 expres- sion, and furthermore that this is expressed in a dorso-ventral gradient in the skin directly comparable to that in mammals8,11,12. Tis potential conservation of agouti signaling protein function is fascinating, since it opens up the possibility of a very diferent cellular mechanism of action in mammals and fsh8,13. Specifcally, we have pro- posed that Asip1 activity in the ventral skin in zebrafsh alters the balance of pigment cell diferentiation, through repressing melanophore diferentiation8. Studies of Asip1 function in fsh to date have relied on gene overexpression approaches, but loss-of-function experiments provide a complementary approach to test the interpretation of those overexpression data. Here, we investigate the in vivo functional role of asip1 in zebrafsh by generating asip1 knockout mutants using clustered regularly interspaced short palindromic repeats (CRISPR)-associated protein-9 nuclease (Cas9) genome engi- neering tools14. We demonstrate that asip1 knockout mutant zebrafsh display a disrupted dorso-ventral pigment pattern characterized, in the ventral region, by an increased number of melanophores and xanthophores accom- panied by a severe decrease in the number of iridophores, i.e. a dorsalised pigment pattern. Tis dorsalisation efect extends also somewhat into the stripes, with the more ventral stripes having melanophore and xanthophore numbers closely resembling their more dorsal counterparts. Our loss-of-function results provide support for our previous hypothesis that asip1 controls the evolutionarily conserved countershading coloration in fsh, but via a distinctive cellular mechanism involving control of diferentiation of multiple pigment cell-types. Results Selection and analysis of induced asip1 loss-of-function mutations in zebrafish. Loss-of- function mutations in the asip1 gene were generated using the CRISPR-Cas9 system. We selected the target site in the frst coding exon (60 bp afer ATG start codon) (Fig. 1A,B) and found ten diferent mutated alleles (Fig. 1B). Alleles M1, M3, M5 and M6 conserved the original open reading frame; therefore, they could potentially generate a functional protein lacking only one or two amino acids and keeping almost the entire amino acid sequence. Alleles M2, M4, M7, M8, M9 and M10 show alternative reading frames downstream of the target site. We selected three potential frameshif mutations, which yield predicted nonfunctional proteins. Fish carrying each mutation were raised to generate asip1K.O. lines (F3 generation) and to characterize the phenotype: M2 (CRISPR1-asip1. iim02 zebrafsh line), M7 (CRISPR1-asip1.iim07 zebrafsh line) and M8 (CRISPR1-asip1.iim08 zebrafsh line) (Fig. 1B). Te asip1iim02 allele lacks 11 bp (76–86 bp), the asip1iim07 allele has lost 4 bp (77–81 bp), and asip1iim08 lacks 16 bp (Del 62–76 bp) and carries a 15 bp insertion at position 62 downstream of the predicted ATG start codon (Fig. 1B). In those three alleles, the mutations result in premature stop codons. Te asip1iim02, asip1iim07 and asip1iim08 encode 71, 38 and 31 amino acid mutant proteins, respectively (Fig. 1C). All mutated proteins have lost most of their basic central domain and, most signifcanctly, the C-terminal poly-cysteine domain, which is the crucial region for protein activity15–17. All asip1 knockout mutant zebrafsh lines examined resulted in a similar dorso-ventral pigment phenotype as described below. asip1 function in dorsal-ventral pigment patterning. All three asip1-CRISPR knockout lines exhib- ited a loss of dorso-ventral countershading. Because we did not fnd any diference in the pigment pattern across the three-knockout mutants’ lines, we focused on the study of line CRISPR1-asip1.iim08, here referred to as asip- 1K.O.. In asip1K.O. fsh, melanophores and xanthophores were more numerous in all ventral regions (Fig. 2A–D), including the ventral head (Fig. 2E,F). In WT fsh, melanophores and xanthophores were very limited in the ventral region, and mainly located on the jaw and the posterior belly regions, near the pelvic fns (Fig. 2G). Te WT phenotype shows a low number of melanophores in the ventral head region and high number of iridophores around the branchiostegals and operculum (Fig. 2E). In contrast, asip1K.O. mutants show melanophores spread throughout the jaws, branchiostegal and opercular regions (Fig. 2F). On the belly, the ventral skin of WT fsh showed almost a total absence of melanophores, so that the bright whitish-refective iridophore sheet of the inter- nal abdominal wall is prominent (Fig. 2G). Conversely, asip1K.O. fsh displayed a strong increase in melanophore and xanthophore number in the ventral skin, as well as many extra cells that transform the incipient 3 V of the WT into a prominent 3 V reaching to the head in the asip1K.O. (Fig. 2A–D). We note that the
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